Colonic mucosa-associated diffusely adherent afaC+ Escherichia coli expressing lpfA and pks are increased in inflammatory bowel disease and colon cancer
Open accessAbstract
OBJECTIVE: Colonic mucosa-associated Escherichia coli are increased in Crohn's disease (CD) and colorectal cancer (CRC). They variously haemagglutinate, invade epithelial cell lines, replicate within macrophages, translocate across M (microfold) cells and damage DNA. We investigated genes responsible for these effects and their co-association in colonic mucosal isolates. DESIGN: A fosmid library yielding 968 clones was prepared in E coli EPI300-T1 using DNA from a haemagglutinating CRC isolate, and resulting haemagglutinating clones were 454-pyrosequenced. PCR screening was performed on 281 colonic E coli isolates from inflammatory bowel disease (IBD) (35 patients), CRC (21) and controls (24; sporadic polyps or irritable bowel syndrome). RESULTS: 454-Pyrosequencing of fosmids from the haemagglutinating clones (n=8) identified the afimbrial adhesin afa-1 operon. Transfection of afa-1 into E coli K-12 predictably conferred diffuse adherence plus invasion of HEp-2 and I-407 epithelial cells, and upregulation of vascular endothelial growth factor. E coli expressing afaC were common in CRC (14/21, p=0.0009) and CD (9/14, p=0.005) but not ulcerative colitis (UC; 8/21) compared with controls (4/24). E coli expressing both afaC and lpfA (relevant to M-cell translocation) were common in CD (8/14, p=0.0019) and CRC (14/21, p=0.0001), but not UC (6/21) compared with controls (2/24). E coli expressing both afaC and pks (genotoxic) were common in CRC (11/21, p=0.0015) and UC (8/21, p=0.022), but not CD (4/14) compared with controls (2/24). All isolates expressed dsbA and htrA relevant to intra-macrophage replication, and 242/281 expressed fimH encoding type-1 fimbrial adhesin. CONCLUSIONS: IBD and CRC commonly have colonic mucosal E coli that express genes that confer properties relevant to pathogenesis including M-cell translocation, angiogenesis and genotoxicity.
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E. coli is overexpressed on colorectal cancer mucosa and expresses genes that confer properties relevant to oncological transformation, including M cell translocation, angiogenesis and genotoxicity.
“E. coli is also overexpressed on CRC mucosa; it expresses genes that confer properties relevant to oncological transformation including M cell translocation, angiogenesis and genotoxicity.96”
From The gut microbiota and host health: a new clinical frontier (2016) · cites this paper as [96]
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- Authors
- Prorok-Hamon, M., Friswell, M. K., Alswied, A., Roberts, C. L., Song, F., Flanagan, P. K., Knight, P., Codling, C., Marchesi, J. R., Winstanley, C., Hall, N., Rhodes, J. M., & Campbell, B. J.
- Affiliations
- University College Cork (IE)
- University of Liverpool (GB)
- Corresponding author
- Campbell, Barry J
- ORCID
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2013-07-11
- Volume
- 63
- Issue
- 5
- Pages
- 761-770
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC3995253
- OpenAlex
- W2114738264
- Cited by
- 236
- References
- 56
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 8 · 2023: 20 · 2022: 17 · 2021: 31 · 2020: 23 · 2019: 16 · 2018: 21 · 2017: 20 · 2016: 19 · 2015: 17 · 2014: 17 · 2013: 2
- FWCI
- 13.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Gut (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institute for Health and Care Research (BRF-2011-025)
- North West Cancer Research
- European Science Foundation
- Science Foundation Ireland
- Crohn's and Colitis UK
- Medical Research Council (MR/K002279/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- Escherichia coli, PKS, inflammatory bowel disease, Crohn's disease, ulcerative colitis, colorectal cancer, colonic mucosa, hemagglutination, diffuse adherence, intracellular replication, genotoxicity, DNA damage, vascular endothelial growth factor
- MeSH terms
- Base Sequence, Cell Line, Colon, Colonic Neoplasms, DNA, Bacterial, Escherichia coli, Hemagglutinins, Humans, Intestinal Mucosa, Molecular Sequence Data, Inflammatory Bowel Diseases, Biomarkers, Case-Control Studies, Sequence Analysis, DNA, Adhesins, Escherichia coli, Caco-2 Cells, Escherichia coli Proteins, Fimbriae Proteins, Polyketide Synthases, Real-Time Polymerase Chain Reaction
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